Opioid modulation of social play reward in juvenile rats
Open accessAbstract
Social play behaviour is a vigorous form of social interaction abundant during the juvenile and adolescent phases of life in many mammalian species, including rats and humans. Social play is thought to be important for social, emotional and cognitive development. Being a rewarding activity, the expression of social play depends on its pleasurable and motivational properties. Since opioids have been widely implicated in reward processes, in the present study we investigated the role of opioids in the pleasurable and motivational properties of social play behaviour in rats. To assess social play motivation, an operant conditioning setup was used in which rats responded for social play under a progressive ratio schedule of reinforcement. Treatment with the opioid receptor agonist morphine reduced responding for social play at the highest dose tested, likely due to its rate-limiting effects. Morphine treatment increased the expression of social play behaviour during reinforced periods. The acquisition of social play-induced conditioned place preference (CPP) in a subeffective conditioning protocol was enhanced by treatment with morphine. Morphine treatment alone also induced CPP. In contrast, antagonizing opioid receptors with naloxone reduced responding for social play, the expression of social play and blocked the development of social play-induced CPP. These data implicate opioid neurotransmission in both the pleasurable and the motivational aspects of social play behaviour in…
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Whereas androgens may set a base frequency of play, other circulating hormones and neurotransmitters, such as endogenous opioids, can modulate how much rats play depending on social context.
“This suggests that whereas androgens may set a base frequency of play, other circulating hormones and neurotransmitters, such as endogenous opioids (Achterberg et al. 2019; Vanderschuren et al. 1995), can modulate how much rats play depending on the social context in which they find themselves (Achterberg et al. 2023).”
From Partner Choice and Context‐Dependent Sex Differences in Rat Rough‐and‐Tumble Play (2026) · cites this paper as Achterberg et al. 2019
Opioid systems have been implicated in the rewards derived from engaging in play.
“While opioid systems have been implicated in the rewards derived from engaging in play (Vanderschuren et al., 2016; Achterberg et al., 2019)”
From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Achterberg et al., 2019
Cites
Dissecting components of reward: ‘liking’, ‘wanting’, and learning
Berridge, K. C., Robinson, T. E., & Aldridge, J. W. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.014 · Cited by 1,942 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468 · see citing works
Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263 · see citing works
Self-citationSex-specific modulation of juvenile social play by vasopressin
Veenema, A. H., Bredewold, R., & De Vries, G. J. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.06.002 · Cited by 166 · cited 1× · see citing works
“Another factor to be pointed out is that both strain and sex differences have been reported in both social play behaviour (e.g. Bredewold et al., 2014; Veenema et al., 2013), the behavioural effects of opioid drugs (Manduca et al.”
Thiel, K. J., Okun, A. C., & Neisewander, J. L. (2008) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2008.02.013 · Cited by 164 · see citing works
Opiate antagonists improve spatial memory
Gallagher, M., King, R. A., & Young, N. B. (1983) · Science · doi:10.1126/science.6879198 · Cited by 159 · see citing works
Aggressive behaviors in adult rats deprived of playfighting experience as juveniles
Potegal, M., & Einon, D. (1989) · Developmental Psychobiology · doi:10.1002/dev.420220206 · Cited by 133 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dopamine Circuit Mechanisms of Addiction-Like Behaviors
Poisson, C. L., Engel, L., & Saunders, B. T. (2021) · Frontiers in Neural Circuits · doi:10.3389/fncir.2021.752420 · Cited by 75 · see citing works
The neurobiology of social play behaviour: Past, present and future
Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105319 · Cited by 56 · see citing works
Self-citationThe rough-and-tumble play of rats as a natural behavior suitable for studying the social brain
Pellis, S. M., Pellis, V. C., Ham, J. R., & Achterberg, E. J. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.1033999 · Cited by 29 · see citing works
“While opioid systems have been implicated in the rewards derived from engaging in play (Vanderschuren et al., 2016; Achterberg et al., 2019), exactly which neural circuits are associated with what types of playful actions and styles of play remains to be investigated.”
BackgroundSelf-citationBredewold, R., Washington, C., & Veenema, A. H. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-024-01987-z · Cited by 13 · see citing works
Neurexin1α knockout in rats causes aberrant social behaviour: relevance for autism and schizophrenia
Achterberg, E. J. M., Biemans, B., & Vanderschuren, L. J. M. J. (2025) · Psychopharmacology · doi:10.1007/s00213-024-06559-z · Cited by 9 · see citing works
Self-citationPartner Choice and Context‐Dependent Sex Differences in Rat Rough‐and‐Tumble Play
Ham, J. R., Pellis, S. M., & McDonald, R. J. (2026) · European Journal of Neuroscience · doi:10.1111/ejn.70426 · Cited by 1 · see citing works
“This suggests that whereas androgens may set a base frequency of play, other circulating hormones and neurotransmitters, such as endogenous opioids (Achterberg et al. 2019; Vanderschuren et al. 1995), can modulate how much rats play depending on the social context in which they find themselves…”
- Authors
- Achterberg, E. J. M., van Swieten, M. M. H., Houwing, D. J., Trezza, V., & Vanderschuren, L. J. M. J.
- Affiliations
- Utrecht University (NL)
- Roma Tre University (IT)
- Corresponding author
- Achterberg, E.J.M.
- Venue
- Neuropharmacology
- Publisher
- Elsevier BV
- Published
- 2019-11
- Volume
- 159
- Pages
- 107332
- ISSN
- 0028-3908 (ISSN-L)
- OpenAlex
- W2891592518
- Cited by
- 52
- References
- 8
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 12 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 6 · 2019: 4
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- green
- dspace.library.uu.nl
- Licence
- Locations
- Neuropharmacology (publishedVersion)
- PubMed (publishedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Iris (Roma Tre University) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Utrecht University
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- social play, opioid modulation, reward, motivation, morphine, naloxone, conditioned place preference, progressive ratio schedule, young rats, opioid receptors, social behavior development
- MeSH terms
- Age Factors, Analgesics, Opioid, Animals, Conditioning, Operant, Dose-Response Relationship, Drug, Interpersonal Relations, Male, Narcotic Antagonists, Play and Playthings, Random Allocation, Reward, Self Administration, Rats, Wistar, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
